Regional specificity of manganese accumulation and clearance in the mouse brain: Implications for manganese-enhanced MRI

NMR in Biomedicine

Volumn 26, Issue 5, 2013, Pages 542-556

  Grunecker B ^a   Kaltwasser, S F ^a   Zappe, A C ^a   Bedenk, B T ^a   Bicker, Y ^a   Spoormaker, V I ^a   Wotjak, C T ^a   Czisch, M ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Accumulation; Half life; Hippocampus dependent learning; Manganese enhanced MRI (MEMRI); Mn2+

Indexed keywords

ACCUMULATION; APPLICATION PROTOCOLS; HALF-LIFE; HIPPOCAMPAL FORMATION; HIPPOCAMPUS-DEPENDENT LEARNING; MANGANESE ACCUMULATION; MANGANESE-ENHANCED MRI; NEURONAL ACTIVITIES;

BRAIN; MANGANESE; NEUROIMAGING; PARAMAGNETISM; TISSUE;

CHLORINE COMPOUNDS;

MANGANESE; MANGANESE CHLORIDE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN ATROPHY; BRAIN SIZE; BRAIN STEM; CEREBELLUM; DENTATE GYRUS; DRUG CLEARANCE; ENTORHINAL CORTEX; GLOBUS PALLIDUS; HIPPOCAMPUS; INFERIOR COLLICULUS; LEARNING; MEMORY DISORDER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEUS ACCUMBENS; OLFACTORY BULB; PRIORITY JOURNAL; PYRIFORM CORTEX; STRIA TERMINALIS; SUPERIOR COLLICULUS; THALAMUS;

ANIMALS; BRAIN; CHLORIDES; IMAGE ENHANCEMENT; MAGNETIC RESONANCE IMAGING; MALE; MANGANESE COMPOUNDS; METABOLIC CLEARANCE RATE; MICE; MICE, INBRED C57BL;

ANIMALIA;

EID: 84876813890     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2891     Document Type: Article

References (57)

1. Pautler RG, Mongeau R, Jacobs RE. In vivo trans-synaptic tract tracing from the murine striatum and amygdala utilizing manganese enhanced MRI (MEMRI). Magn. Reson. Med. 2003; 50: 33-39.
2. Haapanen A, Ramadan UA, Autti T, Joensuu R, Tyynela J. In vivo MRI reveals the dynamics of pathological changes in the brains of cathepsin D-deficient mice and correlates changes in manganese-enhanced MRI with microglial activation. Magn. Reson. Imaging 2007; 25: 1024-1031.
3. Henning EC, Meng X, Fisher M, Sotak CH. Visualization of cortical spreading depression using manganese-enhanced magnetic resonance imaging. Magn. Reson. Med. 2005; 53: 851-857.
4. Golub Y, Kaltwasser SF, Mauch CP, Herrmann L, Schmidt U, Holsboer F, Czisch M, Wotjak CT. Reduced hippocampus volume in the mouse model of posttraumatic stress disorder. J. Psychiatr. Res. 2011; 45: 650-659.
5. 2+-induced contrast. Magn. Reson. Med. 2001; 46: 424-429.
6. Lee JW, Park JA, Lee JJ, Bae SJ, Lee SH, Jung JC, Kim MN, Lee J, Woo S, Chang Y. Manganese-enhanced auditory tract-tracing MRI with cochlear injection. Magn. Reson. Imaging 2007; 25: 652-656.
7. Drapeau P, Nachshen DA. Manganese fluxes and manganese-dependent neurotransmitter release in presynaptic nerve endings isolated from rat brain. J. Physiol. 1984; 348: 493-510.
8. 2+ quench of fura 2 fluorescence. Eur. J. Neurosci. 1995; 7: 831-840.
9. Pautler RG, Koretsky AP. Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. Neuroimage 2002; 16: 441-448.
10. Sloot WN, Gramsbergen JB. Axonal transport of manganese and its relevance to selective neurotoxicity in the rat basal ganglia. Brain Res. 1994; 657: 124-132.
11. Pautler RG, Silva AC, Koretsky AP. In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn. Reson. Med. 1998; 40: 740-748.
12. Van der Linden A, Van Meir V, Tindemans I, Verhoye M, Balthazart J. Applications of manganese-enhanced magnetic resonance imaging (MEMRI) to image brain plasticity in song birds. NMR Biomed. 2004; 17: 602-612.
13. Sun SW, Campbell B, Lunderville C, Won E, Liang HF. Noninvasive topical loading for manganese-enhanced MRI of the mouse visual system. Invest. Ophthalmol. Vis. Sci. 2011; 52: 3914-3920.
14. Massaad CA, Pautler RG. Manganese-enhanced magnetic resonance imaging (MEMRI). Methods Mol. Biol. 2011; 711: 145-174.
15. Chan KC, Cheng JS, Fan S, Zhou IY, Yang J, Wu EX. In vivo evaluation of retinal and callosal projections in early postnatal development and plasticity using manganese-enhanced MRI and diffusion tensor imaging. Neuroimage, 2012; 59: 2274-2283.
16. Chan KC, Li J, Kau P, Zhou IY, Cheung MM, Lau C, Yang J, So KF, Wu EX. In vivo retinotopic mapping of superior colliculus using manganese-enhanced magnetic resonance imaging. Neuroimage, 2011; 54: 389-395.
17. Yu X, Zou J, Babb JS, Johnson G, Sanes DH, Turnbull DH. Statistical mapping of sound-evoked activity in the mouse auditory midbrain using Mn-enhanced MRI. Neuroimage 2008; 39: 223-230.
18. So PW, Yu WS, Kuo YT, Wasserfall C, Goldstone AP, Bell JD, Frost G. Impact of resistant starch on body fat patterning and central appetite regulation. PLoS One 2007; e1309(12): 1-8.
19. Weng JC, Chen JH, Yang PF, Tseng WY. Functional mapping of rat barrel activation following whisker stimulation using activity-induced manganese-dependent contrast. Neuroimage 2007; 36: 1179-1188.
20. Bissig D, Berkowitz BA. Same-session functional assessment of rat retina and brain with manganese-enhanced MRI. Neuroimage 2011; 58: 749-760.
21. Silva AC, Lee JH, Aoki I, Koretsky AP. Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 2004; 17: 532-543.
22. Lin YJ, Koretsky AP. Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn. Reson. Med. 1997; 38: 378-388.
23. Takeda A, Kodama Y, Ishiwatari S, Okada S. Manganese transport in the neural circuit of rat CNS. Brain Res. Bull. 1998; 45: 149-152.
24. 2. NMR Biomed. 2003; 16: 252-256.
25. Bock NA, Paiva FF, Silva AC. Fractionated manganese-enhanced MRI. NMR Biomed. 2008; 21: 473-478.
26. Grünecker B, Kaltwasser SF, Peterse Y, Sämann PG, Schmidt MV, Wotjak CT, Czisch M. Fractionated manganese injections: effects on MRI contrast enhancement and physiological measures in C57BL/6 mice. NMR Biomed. 2010; 23: 913-921.
27. Aoki I, Wu YJ, Silva AC, Lynch RM, Koretsky AP. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage 2004; 22: 1046-1059.
28. Eschenko O, Canals S, Simanova I, Beyerlein M, Murayama Y, Logothetis NK. Mapping of functional brain activity in freely behaving rats during voluntary running using manganese-enhanced MRI: implication for longitudinal studies. Neuroimage 2010; 49: 2544-2555.
29. Jackson SJ, Hussey R, Jansen MA, Merrifield GD, Marshall I, MacLullich A, Yau JL, Bast T. Manganese-enhanced magnetic resonance imaging (MEMRI) of rat brain after systemic administration of MnCl: hippocampal signal enhancement without disruption of hippocampus-dependent behavior. Behav. Brain Res. 2011; 216: 293-300.
30. Kim JJ, Fanselow MS. Modality-specific retrograde amnesia of fear. Science 1992; 256: 675-677.
31. 2 administration using osmotic pumps. Contrast Media Mol. Imaging 2012; 4: 426-434.
32. Andersen ME, Dorman DC, Clewell HJ III, Taylor MD, Nong A. Multi-dose-route, multi-species pharmacokinetic models for manganese and their use in risk assessment. J. Toxicol. Environ. Health A 2010; 73: 217-234.
33. Nong A, Taylor MD, Clewell HJ III, Dorman DC, Andersen ME. Manganese tissue dosimetry in rats and monkeys: accounting for dietary and inhaled Mn with physiologically based pharmacokinetic modeling. Toxicol. Sci. 2009; 108: 22-34.
34. Schroeter JD, Nong A, Yoon M, Taylor MD, Dorman DC, Andersen ME, Clewell HJ III. Analysis of manganese tracer kinetics and target tissue dosimetry in monkeys and humans with multi-route physiologically based pharmacokinetic models. Toxicol. Sci. 2011; 120: 481-498.
35. Beckon WN, Parkins C, Maximovich A, Beckon AV. A general approach to modeling biphasic relationships. Environ. Sci. Technol. 2008; 42: 1308-1314.
36. Kamprath K, Wotjak CT. Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn. Mem. 2004; 11: 770-786.
37. 2. Magn. Reson. Med. 2002; 48: 852-859.
38. Verhoeven WM, Egger JI, Kuijpers HJ. Manganese and acute paranoid psychosis: a case report. J Med Case Reports 2011; 146(5): 1-4.
39. Dorman DC, Struve MF, Wong BA, Dye JA, Robertson ID. Correlation of brain magnetic resonance imaging changes with pallidal manganese concentrations in rhesus monkeys following subchronic manganese inhalation. Toxicol. Sci. 2006; 92: 219-227.
40. 2: dose-dependent and temporal evolution of T1 contrast. Magn. Reson. Med. 2005; 53: 640-648.
41. Itoh K, Sakata M, Watanabe M, Aikawa Y, Fujii H. The entry of manganese ions into the brain is accelerated by activation of N-methyl-D-aspartate receptors. Neuroscience 2008; 154: 732-740.
42. Lu H, Xi Z-X, Gitajn L, Rea W, Yang Y, Stein EA. Cocaine-induced brain activation detected by dynamic manganese-enhanced magnetic resonance imaging (MEMRI). Proc. Natl. Acad. Sci. U.S.A. 2007; 104: 2489-2494.
43. Kuo YT, Herlihy AH, So PW, Bhakoo KK, Bell JD. In vivo measurements of T1 relaxation times in mouse brain associated with different modes of systemic administration of manganese chloride. J. Magn. Reson. Imaging 2005; 21: 334-339.
44. Takeda A, Sawashita J, Okada S. Biological half-lives of zinc and manganese in rat brain. Brain Res. 1995; 695: 53-58.
45. 2. Neuroimage 2004; 22: 860-867.
46. Kern CH, Stanwood GD, Smith DR. Preweaning manganese exposure causes hyperactivity, disinhibition, and spatial learning and memory deficits associated with altered dopamine receptor and transporter levels. Synapse 2010; 64: 363-378.
47. Wasserman GA, Liu X, Parvez F, Factor-Litvak P, Ahsan H, Levy D, Kline J, van Geen A, Mey J, Slavkovich V, Siddique AB, Islam T, Graziano JH. Arsenic and manganese exposure and children's intellectual function. Neurotoxicology 2011; 32: 450-457.
48. Talalaenko AN, Krivobok GK, Bulgakova NP, Pankrat'ev DV. Functional roles of the monoaminergic and aminoacidergic mechanisms of the dorsal pallidum in anxiety of different aversive origins. Neurosci. Behav. Physiol. 2008; 38: 115-118.
49. Lucchini R, Apostoli P, Perrone C, Placidi D, Albini E, Migliorati P, Mergler D, Sassine MP, Palmi S, Alessio L. Long-term exposure to "low levels" of manganese oxides and neurofunctional changes in ferroalloy workers. Neurotoxicology 1999; 20: 287-297.
50. Layrargues GP, Shapcott D, Spahr L, Butterworth RF. Accumulation of manganese and copper in pallidum of cirrhotic patients: role in the pathogenesis of hepatic encephalopathy? Metab. Brain Dis. 1995; 10: 353-356.
51. Ikeda S, Yamaguchi Y, Sera Y, Ohshiro H, Uchino S, Yamashita Y, Ogawa M. Manganese deposition in the globus pallidus in patients with biliary atresia. Transplantation 2000; 69: 2339-2343.
52. Erikson KM, Dorman DC, Lash LH, Aschner M. Manganese inhalation by rhesus monkeys is associated with brain regional changes in biomarkers of neurotoxicity. Toxicol. Sci. 2007; 97: 459-466.
53. Gonzalez-Lima F, Cada A. Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study. Neuroscience 1994; 63: 559-578.
54. Dorman DC, Struve MF, Marshall MW, Parkinson CU, James RA, Wong BA. Tissue manganese concentrations in young male rhesus monkeys following subchronic manganese sulfate inhalation. Toxicol. Sci. 2006; 92: 201-210.
55. Han JH, Chung YH, Park JD, Kim CY, Yang SO, Khang HS, Cheong HK, Lee JS, Ha CS, Song CW, Kwon IH, Sung JH, Heo JD, Kim NY, Huang M, Cho MH, Yu IJ. Recovery from welding-fume-exposure-induced MRI T1 signal intensities after cessation of welding-fume exposure in brains of cynomolgus monkeys. Inhal. Toxicol. 2008; 20: 1075-1083.
56. Chuang KH, Koretsky AP, Sotak CH. Temporal changes in the T1 and T2 relaxation rates (DeltaR1 and DeltaR2) in the rat brain are consistent with the tissue-clearance rates of elemental manganese. Magn. Reson. Med. 2009; 61: 1528-1532.
57. Franklin K, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. Academic Press, Inc.: San Diego; 1997.